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. 2020 Sep 3:11:571831.
doi: 10.3389/fmicb.2020.571831. eCollection 2020.

Medusavirus Ancestor in a Proto-Eukaryotic Cell: Updating the Hypothesis for the Viral Origin of the Nucleus

Masaharu Takemura  1
Affiliations

Medusavirus Ancestor in a Proto-Eukaryotic Cell: Updating the Hypothesis for the Viral Origin of the Nucleus

Masaharu Takemura. Front Microbiol. .

Abstract

The mechanistic evolutionary origin of the eukaryotic cell nucleus remains unknown. Among several plausible hypotheses, the most controversial is that large DNA viruses, such as poxviruses, led to the emergence of the eukaryotic cell nucleus. Several recent findings, including the discovery of a nucleus-like structure in prokaryotic viruses and prokaryotes possessing nucleus-like inner membranes, suggest genomic DNA compartmentalization not only in eukaryotes but also in prokaryotes. The sophisticated viral machinery of mimiviruses is thought to resemble the eukaryotic nucleus: DNA replicates both inside the viral factory and nucleus, which is at least partially surrounded by membranes and is devoid of ribosomes. Furthermore, several features of the recently identified Acanthamoeba castellanii medusavirus suggest that the evolutionary relationship between ancestral viral factory and eukaryotic nucleus. Notably, Ran, DNA polymerase, and histones show molecular fossils of lateral transfer of nuclear genes between the virus and host. These results suggest viral innovation in the emergence of the eukaryotic nucleus. According to these results, a new scenario explaining the origin of the eukaryotic nucleus from the perspective of viral participation is proposed. This new scenario could substantially impact the study of eukaryogenesis and stimulate further discussion about viral contributions to the evolution of the eukaryotic nucleus.

Keywords: evolution; giant virus; medusavirus; origin of the nucleus; viral eukaryogenesis.

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Figures

FIGURE 1
FIGURE 1
Properties of medusavirus. (A) Fluorescence image of DAPI-stained acanthamoeba cells with or without the infection of medusavirus. Eight hours post-infection cells were fixed by methanol and stained with 500 ng/mL of DAPI for 50 s, followed by fluorescent microscopic observation, as described previously (Takemura, 2016). (B) Putative scenario of loss and acquisition of several important genes of medusavirus. LGT, lateral gene transfer.
FIGURE 2
FIGURE 2
Hypothetical evolutionary mechanisms of the exclusion system of ribosomes from the nucleus. (A) In a putative ancestral prokaryotic host cell, DNA genome and ribosomes co-exist in proximity, so transcribed rRNA genes can directly construct ribosome particles near DNA because of the absence of intron and splicing system. (B) In a putative ancestral PAM (here hypothesize medusavirus)-infected host cell, DNA genome was separated from ribosomes by the function of putative Ran outside VF, because of the presence of intron and splicing system. This putative VF may have evolved into the eukaryotic nucleus. VF, viral factory.
FIGURE 3
FIGURE 3
New scenario explaining the origin of the eukaryotic nucleus. (A) An ancestral virus of the currently existing giant viruses, PAMs, constructed a VF, which surrounded the viral genome using a cytoplasmic inner membrane (putatively ER)-derived membranes in infected proto-eukaryotic cells. (B) Among these ancestral viruses, viruses replicating its DNA very closely to host genome emerged, putatively ancestral medusavirus. Against this viral “attack,” the host cell developed a defense system to envelope its genome with the inner membrane. (C) This membrane evolved into what nowadays is known as the nuclear membrane. After the emergence of the nucleus, giant viruses infecting eukaryotic cells evolved and diversified to several currently present infection systems. Black genes represent host cell genes, red genes indicate mimivirus lineage genes, and blue genes stand for medusavirus lineage genes. POLB, B family DNA polymerase; RNAP, DNA-dependent RNA polymerase; FECA, the first eukaryotic common ancestor; VF, viral factory.
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